622 Invasive Stink Bugs and Related Species (Pentatomoidea)
E. coryli infection causes cream-colored, sunken areas or necrotic, discolored lesions on the seed coat,
hence the name yeast spot. Infection during pod formation causes abscission; infection during seed
development produces spots, depressions, shriveling, and change in texture and color of the cotyledon.
Preston and Ray (1943) found that lima bean, cowpea, mung bean, and soybean could be affected. The
role of stink bugs in the transmission of this disease on lima beans (as Nematospora phaseoli Wingard)
was confirmed by Wingard (1925), but research on vectors of yeast spot of soybean did not begin until
the 1960s. Prior to this time, the symptoms of yeast infection often had been attributed to direct stink
bug feeding damage (Daugherty 1967).
Daugherty (1967) reported that Thyanta custator ( F.), Euschistus variolarius (Palisot de Beauvois),
E. tristigmus (Say), E. servus euschistoides (Vollenhoven), E. servus servus (Say), and Chinavia hilaris
transmitted yeast spot disease in cage studies in the United States; macerated heads of E. servus ser-
vus were found to contain the fungus. Two other pentatomids, Holcostethus limbolarius (Stål) and
Cosmopepla lintneriana Kirkaldy (as C. bimaculata Thomas), also were tested by Daugherty (1967),
but they failed to transmit the fungus to soybeans. Earlier studies of the disease in lima bean already
had implicated C. hilaris (Wingard 1925, Schoene and Underhill 1933), although Leach and Clulo
(1943) questioned whether the fungus could be carried internally. Subsequently, more detailed studies of
C. hilaris conducted by Foster and Daugherty (1969) yielded viable yeast from surface-sterilized nymphs
and adults, and from all three tagmata of macerated bodies of surface-sterilized adult bugs, although
more frequently from heads and abdomens. Analysis of organs revealed spores to be present primarily
in the stylets, salivary receptacles, and hindgut. Clark and Wilde (1970a,b) studied retention and acquisi-
tion of the fungus. Laboratory inoculation of C. hilaris using a yeast suspension or infected pods showed
retention of Eremothecium coryli for 90 days and at least 60 days, respectively. Heads were more likely
than other body regions to carry the fungus. Viable E. coryli also could be isolated from feces. Fifth
instars lost the ability to transmit after the adult molt, but their exuviae were infective (Clark and Wilde
1970a). Adults could acquire the fungus by feeding on soybean or dogwood (Cornus drummondii Meyer)
berries previously fed upon by infected bugs (Clark and Wilde 1970b). A survey of microorganisms asso-
ciated with Nezara viridula collected from soybean in Louisiana (Ragsdale et al. 1979) showed only 2 of
118 insects tested carried E. coryli internally, although the dimensions of the salivary and food canals in
this species are large enough to admit the ascospores. In Japan, both E. coryli and E. ashbyi cause yeast
spot of soybean (Kimura et al. 2008b). Although research has focused on the primary vector, the alydid
Riptortus pedestris (F.) [as Riptortus clavatus (Thunberg)], several pentatomid species also have been
shown to carry and transmit E. coryli but at lower rates. Transmission rates for adults of N. antennata
Scott, Dolycoris baccarum (L.), and Piezodorus hybneri (Gmelin) were 50.0, 40.0, and 16.7%, respec-
tively, compared with 81.6% for R. pedestris. No E. coryli was isolated from nymphs of N. antennator
or D. baccarum, although the carrying rate for nymphs of R. pedestris was 11.5% (Kimura et al. 2008a).
Fungi other than Eremothecium coryli also are associated with stink bugs on soybean, but the relation-
ship is not as intimate as that for yeast spot. Two Penicillium spp. isolates also were included among the
internal microflora of Nezara viridula (Ragsdale et al. 1979). Seed infection by Fusarium spp. increased
significantly with stink bug feeding damage in controlled field plots in Louisiana (Russin et al. 1988).
In the same study, rates of seedborne Alternaria spp., Colletotrichum truncatum (Schw.) Andrus &
W. D. Moore, and Phomopsis spp. were unaffected by population levels of stink bugs, which included
N. viridula (77.9%), Euschistus spp. (16.6%), and C. hilaris (5.5%) (Russin et al. 1988). However, Nyvall
(1999) noted that infection rates for seedborne Alternaria spp. were associated with damage by bean leaf
beetle and stink bugs. In Brazil, increased seed infection by Fusarium sp., Phomopsis sojae Lehman,
and C. truncatum is associated with feeding by Piezodorus guildinii (Westwood) (Panizzi et al. 1979).
These fungi occur naturally on soybean and can infect seeds in the absence of stink bugs. The role of the
bugs is to alter the incidence of infection; whether this is due to the physical damage from feeding or a
change in nutritional quality of the damaged seed is uncertain (Russin et al. 1988).
13.5.5 Pistachio
In California, several hemipterans cause direct damage to pistachio (Pistacia vera L.) fruits, producing
a condition known as epicarp lesion and characterized by the appearance of necrotic regions followed by